Spray-induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake

Qiao, Lulu; Lan, Chi; Capriotti, Luca; Ah‐Fong, Audrey; Nino Sanchez, Jonatan; Hamby, Rachael; Heller, Jens; Zhao, Hongwei; Glass, N. Louise; Judelson, Howard S.; Mezzetti, Bruno; Niu, Dongdong; Jin, Hailing

doi:10.1111/pbi.13589

Spray-induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake

Journal Article · Sat Mar 27 00:00:00 EDT 2021 · Plant Biotechnology Journal

DOI:https://doi.org/10.1111/pbi.13589· OSTI ID:1784294

Qiao, Lulu ^[1]; Lan, Chi ^[2]; Capriotti, Luca ^[3]; Ah‐Fong, Audrey ^[4]; Nino Sanchez, Jonatan ^[4]; Hamby, Rachael ^[4]; Heller, Jens ^[5]; ^[2]; Glass, N. Louise ^[5]; Judelson, Howard S. ^[4]; Mezzetti, Bruno ^[3]; ^[1]; ^[4]

Nanjing Agricultural University (China); Ministry of Education, Nanjing (China); Univ. of California, Riverside, CA (United States)
Nanjing Agricultural University (China); Ministry of Education, Nanjing (China)
Univ. of California, Riverside, CA (United States); Marche Polytechnic University, Ancona (Italy)
Univ. of California, Riverside, CA (United States)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Recent discoveries show that fungi can take up environmental RNA, which can then silence fungal genes through environmental RNA interference. This discovery prompted the development of Spray-Induced Gene Silencing (SIGS) for plant disease management. In this study, we aimed to determine the efficacy of SIGS across a variety of eukaryotic microbes. We first examined the efficiency of RNA uptake in multiple pathogenic and non-pathogenic fungi, and an oomycete pathogen. We observed efficient double-stranded RNA (dsRNA) uptake in the fungal plant pathogens Botrytis cinerea, Sclerotinia sclerotiorum, Rhizoctonia solani, Aspergillus niger and Verticillium dahliae, but no uptake in Colletotrichum gloeosporioides, and weak uptake in a beneficial fungus, Trichoderma virens. For the oomycete plant pathogen, Phytophthora infestans, RNA uptake was limited and varied across different cell types and developmental stages. Topical application of dsRNA targeting virulence-related genes in pathogens with high RNA uptake efficiency significantly inhibited plant disease symptoms, whereas the application of dsRNA in pathogens with low RNA uptake efficiency did not suppress infection. Our results have revealed that dsRNA uptake efficiencies vary across eukaryotic microbe species and cell types. The success of SIGS for plant disease management can largely be determined by the pathogen's RNA uptake efficiency.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Science Foundation (NSF); USDA; National Institute of Food and Agriculture (NIFA); Australian Research Council (ARC); Canadian Institute for Advanced Research (CIFAR); Jiangsu Agricultural Science and Technology Innovation Fund of China

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1784294

Journal Information:: Plant Biotechnology Journal, Journal Name: Plant Biotechnology Journal Journal Issue: 9 Vol. 19; ISSN 1467-7644

Publisher:: Society for Experimental Biology; Association of Applied BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (66)

The structure and synthesis of the fungal cell wall Bowman, Shaun M.; Free, Stephen J. BioEssays, Vol. 28, Issue 8 https://doi.org/10.1002/bies.20441	journal	January 2006
Exogenous nitric oxide-induced postharvest disease resistance in citrus fruit to Colletotrichum gloeosporioides : Effect of NO on disease resistance in citrus fruit Zhou, Yahan; Li, Shunmin; Zeng, Kaifang Journal of the Science of Food and Agriculture, Vol. 96, Issue 2 https://doi.org/10.1002/jsfa.7117	journal	April 2015
Phytophthora infestans: populations, pathogenicity and phenylamides Shattock, Richard C. Pest Management Science, Vol. 58, Issue 9 https://doi.org/10.1002/ps.527	journal	January 2002
RNA‐based biocontrol compounds: current status and perspectives to reach the market Taning, Clauvis NT; Arpaia, Salvatore; Christiaens, Olivier Pest Management Science, Vol. 76, Issue 3 https://doi.org/10.1002/ps.5686	journal	October 2019
Alterations in the cell wall ofSaccharomyces cerevisiae induced by the alpha sex factor or a mutation in the cell cycle D�az, Silvia; Z�nker, Samuel; Ruiz-Herrera, Jos� Antonie van Leeuwenhoek, Vol. 61, Issue 4 https://doi.org/10.1007/BF00713935	journal	May 1992
Interactions between Verticillium dahliae and its host: vegetative growth, pathogenicity, plant immunity Luo, Xiumei; Xie, Chengjian; Dong, Jinyan Applied Microbiology and Biotechnology, Vol. 98, Issue 16 https://doi.org/10.1007/s00253-014-5863-8	journal	June 2014
Control of brown patch (Rhizoctonia solani) in tall fescue (Festuca arundinacea Schreb.) by host induced gene silencing Zhou, Binbin; Bailey, Ana; Niblett, C. L. Plant Cell Reports, Vol. 35, Issue 4 https://doi.org/10.1007/s00299-015-1921-7	journal	January 2016
Pectin induced transcriptome of a Rhizoctonia solani strain causing sheath blight disease in rice reveals insights on key genes and RNAi machinery for development of pathogen derived resistance Rao, Talluri Bhaskar; Chopperla, Ramakrishna; Methre, Ramesh Plant Molecular Biology, Vol. 100, Issue 1-2 https://doi.org/10.1007/s11103-019-00843-9	journal	February 2019
RNA-based technologies for insect control in plant production Liu, Shaoshuai; Jaouannet, Maelle; Dempsey, D'Maris Amick Biotechnology Advances, Vol. 39 https://doi.org/10.1016/j.biotechadv.2019.107463	journal	March 2020
Small RNAs – Big Players in Plant-Microbe Interactions Huang, Chien-Yu; Wang, Huan; Hu, Po Cell Host & Microbe, Vol. 26, Issue 2 https://doi.org/10.1016/j.chom.2019.07.021	journal	August 2019
Impact on environment, ecosystem, diversity and health from culturing and using GMOs as feed and food Tsatsakis, Aristidis M.; Nawaz, Muhammad Amjad; Tutelyan, Victor A. Food and Chemical Toxicology, Vol. 107 https://doi.org/10.1016/j.fct.2017.06.033	journal	September 2017
Surveying selected European feed and livestock production chains for features enabling the case-specific post-market monitoring of livestock for intake and potential health impacts of animal feeds derived from genetically modified crops Kleter, Gijs; McFarland, Sarah; Bach, Alex Food and Chemical Toxicology, Vol. 117 https://doi.org/10.1016/j.fct.2017.10.004	journal	July 2018
Crop-destroying fungal and oomycete pathogens challenge food security Bebber, Daniel P.; Gurr, Sarah J. Fungal Genetics and Biology, Vol. 74 https://doi.org/10.1016/j.fgb.2014.10.012	journal	January 2015
Fungi and mycotoxins in vineyards and grape products Hocking, Ailsa D.; Leong, Su-lin L.; Kazi, Benozir A. International Journal of Food Microbiology, Vol. 119, Issue 1-2 https://doi.org/10.1016/j.ijfoodmicro.2007.07.031	journal	October 2007
Cross-kingdom RNA trafficking and environmental RNAi — nature's blueprint for modern crop protection strategies Cai, Qiang; He, Baoye; Kogel, Karl-Heinz Current Opinion in Microbiology, Vol. 46 https://doi.org/10.1016/j.mib.2018.02.003	journal	December 2018
Characterization of the cell wall of the ubiquitous plant pathogen Botrytis cinerea Cantu, Dario; Carl Greve, L.; Labavitch, John M. Mycological Research, Vol. 113, Issue 12 https://doi.org/10.1016/j.mycres.2009.09.006	journal	December 2009
Antifungal activity of nano and micro charcoal particle polymers against Paecilomyces variotii, Trichoderma virens and Chaetomium globosum Yang, Hee Jin; Cha, Yun Jeong; Kim, Hern New Biotechnology, Vol. 33, Issue 1 https://doi.org/10.1016/j.nbt.2015.08.001	journal	January 2016
Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection Wang, Ming; Thomas, Nicholas; Jin, Hailing Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.05.003	journal	August 2017
Comparison of efficacy of RNAi mediated by various nanoparticles in the rice striped stem borer (Chilo suppressalis) Wang, Kangxu; Peng, Yingchuan; Chen, Jiasheng Pesticide Biochemistry and Physiology, Vol. 165 https://doi.org/10.1016/j.pestbp.2019.10.005	journal	May 2020
Pathogenic attributes of Sclerotinia sclerotiorum : Switching from a biotrophic to necrotrophic lifestyle Kabbage, Mehdi; Yarden, Oded; Dickman, Martin B. Plant Science, Vol. 233 https://doi.org/10.1016/j.plantsci.2014.12.018	journal	April 2015
Real-time PCR monitoring of fungal development in Arabidopsis thaliana infected by Alternaria brassicicola and Botrytis cinerea Gachon, Claire; Saindrenan, Patrick Plant Physiology and Biochemistry, Vol. 42, Issue 5 https://doi.org/10.1016/j.plaphy.2004.04.001	journal	May 2004
Spray-Induced Gene Silencing: a Powerful Innovative Strategy for Crop Protection Wang, Ming; Jin, Hailing Trends in Microbiology, Vol. 25, Issue 1 https://doi.org/10.1016/j.tim.2016.11.011	journal	January 2017
Control of coleopteran insect pests through RNA interference Baum, James A.; Bogaert, Thierry; Clinton, William Nature Biotechnology, Vol. 25, Issue 11 https://doi.org/10.1038/nbt1359	journal	November 2007
The evolution and pathogenic mechanisms of the rice sheath blight pathogen Zheng, Aiping; Lin, Runmao; Zhang, Danhua Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2427	journal	January 2013
Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection Wang, Ming; Weiberg, Arne; Lin, Feng-Mao Nature Plants, Vol. 2, Issue 10 https://doi.org/10.1038/nplants.2016.151	journal	September 2016
Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen Zhang, Tao; Zhao, Yun-Long; Zhao, Jian-Hua Nature Plants, Vol. 2, Issue 10 https://doi.org/10.1038/nplants.2016.153	journal	September 2016
Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses Mitter, Neena; Worrall, Elizabeth A.; Robinson, Karl E. Nature Plants, Vol. 3, Issue 2 https://doi.org/10.1038/nplants.2016.207	journal	January 2017
Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea McLoughlin, Austein G.; Wytinck, Nick; Walker, Philip L. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-25434-4	journal	May 2018
RNA silencing is required for Arabidopsis defence against Verticillium wilt disease Ellendorff, Ursula; Fradin, Emilie F.; de Jonge, Ronnie Journal of Experimental Botany, Vol. 60, Issue 2 https://doi.org/10.1093/jxb/ern306	journal	December 2008
Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans Jahan, Sultana N.; Åsman, Anna K. M.; Corcoran, Pádraic Journal of Experimental Botany, Vol. 66, Issue 9 https://doi.org/10.1093/jxb/erv094	journal	March 2015
The Sclerotinia sclerotiorum pac1 Gene Is Required for Sclerotial Development and Virulence Rollins, Jeffrey A. Molecular Plant-Microbe Interactions®, Vol. 16, Issue 9 https://doi.org/10.1094/MPMI.2003.16.9.785	journal	September 2003
Potato and Tomato Late Blight Caused by Phytophthora infestans : An Overview of Pathology and Resistance Breeding Nowicki, Marcin; Foolad, Majid R.; Nowakowska, Marzena Plant Disease, Vol. 96, Issue 1 https://doi.org/10.1094/PDIS-05-11-0458	journal	January 2012
How Does Phytophthora infestans Evade Control Efforts? Modern Insight Into the Late Blight Disease Leesutthiphonchai, Wiphawee; Vu, Andrea L.; Ah-Fong, Audrey M. V. Phytopathology®, Vol. 108, Issue 8 https://doi.org/10.1094/PHYTO-04-18-0130-IA	journal	August 2018
Trichoderma virens , a Plant Beneficial Fungus, Enhances Biomass Production and Promotes Lateral Root Growth through an Auxin-Dependent Mechanism in Arabidopsis Contreras-Cornejo, Hexon Angel; Macías-Rodríguez, Lourdes; Cortés-Penagos, Carlos Plant Physiology, Vol. 149, Issue 3 https://doi.org/10.1104/pp.108.130369	journal	January 2009
HIGS: Host-Induced Gene Silencing in the Obligate Biotrophic Fungal Pathogen Blumeria graminis Nowara, Daniela; Gay, Alexandra; Lacomme, Christophe The Plant Cell, Vol. 22, Issue 9 https://doi.org/10.1105/tpc.110.077040	journal	September 2010
Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen Bolton, Melvin D.; Thomma, Bart P. H. J.; Nelson, Berlin D. Molecular Plant Pathology, Vol. 7, Issue 1 https://doi.org/10.1111/j.1364-3703.2005.00316.x	journal	January 2006
Evidence for involvement of Dicer-like, Argonaute and histone deacetylase proteins in gene silencing in Phytophthora infestans: Gene silencing in Phytophthora infestans Vetukuri, Ramesh R.; Avrova, Anna O.; Grenville-Briggs, Laura J. Molecular Plant Pathology, Vol. 12, Issue 8 https://doi.org/10.1111/j.1364-3703.2011.00710.x	journal	March 2011
A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato Avrova, Anna O.; Boevink, Petra C.; Young, Vanessa Cellular Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-5822.2008.01206.x	journal	November 2008
Host-induced gene silencing compromises Verticillium wilt in tomato and Arabidopsis: HIGS against Verticillium wilt Song, Yin; Thomma, Bart P. H. J. Molecular Plant Pathology, Vol. 19, Issue 1 https://doi.org/10.1111/mpp.12500	journal	December 2016
Secondary amplification of siRNA machinery limits the application of spray-induced gene silencing: Secondary siRNA amplification limits SIGS Song, Xiu-Shi; Gu, Kai-Xin; Duan, Xiao-Xin Molecular Plant Pathology, Vol. 19, Issue 12 https://doi.org/10.1111/mpp.12728	journal	September 2018
New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing Koch, Aline; Kogel, Karl-Heinz Plant Biotechnology Journal, Vol. 12, Issue 7 https://doi.org/10.1111/pbi.12226	journal	July 2014
Host‐induced gene silencing inhibits the biotrophic pathogen causing downy mildew of lettuce Govindarajulu, Manjula; Epstein, Lynn; Wroblewski, Tadeusz Plant Biotechnology Journal, Vol. 13, Issue 7 https://doi.org/10.1111/pbi.12307	journal	December 2014
Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae Abdellatef, Eltayb; Will, Torsten; Koch, Aline Plant Biotechnology Journal, Vol. 13, Issue 6 https://doi.org/10.1111/pbi.12322	journal	January 2015
Host-induced gene silencing of a regulator of G protein signalling gene ( VdRGS1 ) confers resistance to Verticillium wilt in cotton Xu, Jun; Wang, Xinyu; Li, Yongqing Plant Biotechnology Journal, Vol. 16, Issue 9 https://doi.org/10.1111/pbi.12900	journal	March 2018
Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways Weiberg, Arne; Wang, Ming; Lin, Feng-Mao Science, Vol. 342, Issue 6154 https://doi.org/10.1126/science.1239705	journal	October 2013
Worldwide emergence of resistance to antifungal drugs challenges human health and food security Fisher, Matthew C.; Hawkins, Nichola J.; Sanglard, Dominique Science, Vol. 360, Issue 6390 https://doi.org/10.1126/science.aap7999	journal	May 2018
Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes Cai, Qiang; Qiao, Lulu; Wang, Ming Science, Vol. 360, Issue 6393 https://doi.org/10.1126/science.aar4142	journal	May 2018
Analyses of Extracellular Carbohydrates in Oomycetes Unveil the Existence of Three Different Cell Wall Types Mélida, Hugo; Sandoval-Sierra, Jose V.; Diéguez-Uribeondo, Javier Eukaryotic Cell, Vol. 12, Issue 2 https://doi.org/10.1128/EC.00288-12	journal	November 2012
A Phytophthora infestans G-Protein β Subunit Is Involved in Sporangium Formation Latijnhouwers, Maita; Govers, Francine Eukaryotic Cell, Vol. 2, Issue 5 https://doi.org/10.1128/EC.2.5.971-977.2003	journal	October 2003
The Viscoelastic Properties of the Fungal Cell Wall Allow Traffic of AmBisome as Intact Liposome Vesicles Walker, Louise; Sood, Prashant; Lenardon, Megan D. mBio, Vol. 9, Issue 1 https://doi.org/10.1128/mBio.02383-17	journal	February 2018
Diversity, Pathogenicity, and Management of Verticillium Species Klosterman, Steven J.; Atallah, Zahi K.; Vallad, Gary E. Annual Review of Phytopathology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-phyto-080508-081748	journal	September 2009
RNA-seq of life stages of the oomycete Phytophthora infestans reveals dynamic changes in metabolic, signal transduction, and pathogenesis genes and a major role for calcium signaling in development Ah-Fong, Audrey M. V.; Kim, Kyoung Su; Judelson, Howard S. BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3585-x	journal	February 2017
Overexpression of a Defensin Enhances Resistance to a Fruit-Specific Anthracnose Fungus in Pepper Seo, Hyo-Hyoun; Park, Sangkyu; Park, Soomin PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0097936	journal	May 2014
An ANNEXIN-Like Protein from the Cereal Cyst Nematode Heterodera avenae Suppresses Plant Defense Chen, Changlong; Liu, Shusen; Liu, Qian PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0122256	journal	April 2015
Polygalacturonase gene pgxB in Aspergillus niger is a virulence factor in apple fruit Liu, Cheng-Qian; Hu, Kang-Di; Li, Ting-Ting PLOS ONE, Vol. 12, Issue 3 https://doi.org/10.1371/journal.pone.0173277	journal	March 2017
An RNAi-Based Control of Fusarium graminearum Infections Through Spraying of Long dsRNAs Involves a Plant Passage and Is Controlled by the Fungal Silencing Machinery Koch, Aline; Biedenkopf, Dagmar; Furch, Alexandra PLOS Pathogens, Vol. 12, Issue 10 https://doi.org/10.1371/journal.ppat.1005901	journal	October 2016
Small RNAs and extracellular vesicles: New mechanisms of cross-species communication and innovative tools for disease control Cai, Qiang; He, Baoye; Weiberg, Arne PLOS Pathogens, Vol. 15, Issue 12 https://doi.org/10.1371/journal.ppat.1008090	journal	December 2019
Liposomes as siRNA Delivery Vectors Bochicchio, Sabrina; Dalmoro, Annalisa; Barba, Anna Current Drug Metabolism, Vol. 15, Issue 9 https://doi.org/10.2174/1389200216666150206124913	journal	March 2015
Dicer-like Proteins Regulate the Growth, Conidiation, and Pathogenicity of Colletotrichum gloeosporioides from Hevea brasiliensis Wang, Qiannan; An, Bang; Hou, Xingrong Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02621	journal	January 2018
Host-Induced Silencing of Two Pharyngeal Gland Genes Conferred Transcriptional Alteration of Cell Wall-Modifying Enzymes of Meloidogyne incognita vis-à-vis Perturbed Nematode Infectivity in Eggplant Shivakumara, Tagginahalli N.; Chaudhary, Sonam; Kamaraju, Divya Frontiers in Plant Science, Vol. 08 https://doi.org/10.3389/fpls.2017.00473	journal	March 2017
sRNA Profiling Combined With Gene Function Analysis Reveals a Lack of Evidence for Cross-Kingdom RNAi in the Wheat – Zymoseptoria tritici Pathosystem Kettles, Graeme J.; Hofinger, Bernhard J.; Hu, Pingsha Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00892	journal	July 2019
Host-Induced Gene Silencing: A Powerful Strategy to Control Diseases of Wheat and Barley Qi, Tuo; Guo, Jia; Peng, Huan International Journal of Molecular Sciences, Vol. 20, Issue 1 https://doi.org/10.3390/ijms20010206	journal	January 2019
Biotechnological Approaches: Gene Overexpression, Gene Silencing, and Genome Editing to Control Fungal and Oomycete Diseases in Grapevine Capriotti, Luca; Baraldi, Elena; Mezzetti, Bruno International Journal of Molecular Sciences, Vol. 21, Issue 16 https://doi.org/10.3390/ijms21165701	journal	August 2020
Consumer Perception of Genetically Modified Organisms and Sources of Information Wunderlich, Shahla; Gatto, Kelsey A. Advances in Nutrition, Vol. 6, Issue 6 https://doi.org/10.3945/an.115.008870	journal	November 2015
Trichoderma -induced plant immunity likely involves both hormonal- and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea . Contreras-Cornejo, Hexon Angel; Macías-Rodríguez, Lourdes; Beltrán-Peña, Elda Plant Signaling & Behavior, Vol. 6, Issue 10 https://doi.org/10.4161/psb.6.10.17443	journal	October 2011
Additional file 2: of RNA-seq of life stages of the oomycete Phytophthora infestans reveals dynamic changes in metabolic, signal transduction, and pathogenesis genes and a major role for calcium signaling in development Ah-Fong, Audrey; Kim, Kyoung; Judelson, Howard Figshare https://doi.org/10.6084/m9.figshare.c.3700951_d4.v1	dataset	January 2017

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59 BASIC BIOLOGICAL SCIENCES
RNA interference
double-stranded RNA
small RNA
spray-induced gene silencing
uptake efficiency

Spray-induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake

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